https://doi.org/10.1130/G48788.1 Manuscript received 5 January 2021 Revised manuscript received 30 March 2021 Manuscript accepted 1 April 2021 © 2021 The Authors. Gold Open Access: This paper is published under the terms of the CC-BY license. Published online 3 June 2021 Morphological selectivity of the Permian-Triassic ammonoid mass extinction Xu Dai1, Dieter Korn2 and Haijun Song1* 1 State Key Laboratory of Biogeology and Environmental Geology, School of Earth Sciences, China University of Geosciences, Wuhan 430074, China 2 Museum für Naturkunde Berlin, Leibniz-Institut für Evolutions- und Biodiversitätsforschung, Invalidenstraße 43, 10115 Berlin, Germany ABSTRACT lineages, episageceratids, xenodiscids, and otoc- Ammonoids suffered a diversity bottleneck during the Permian-Triassic mass extinction eratids (Wiedmann, 1973; Teichert and Roches- (PTME) and experienced a rapid diversification in the Early Triassic. However, the kinds of ter, 1986; Brayard et al., 2009). The PTME was ammonoids that were more likely to survive the PTME and that fueled subsequent diversi- thought to be nonselective in terms of ammonoid fication are still poorly known. We compiled a comprehensive morphological data set and conch morphology, because geometric ratios of used the nonmetric multidimensional scaling method to reveal the impact of the PTME on ammonoid conchs showed little change across the morphological selectivity of ammonoids. Our results show that postextinction taxa oc- the PTME (Villier and Korn, 2004; Korn et al., cupied a quite different morphospace when compared with the pre-extinction assemblages. 2013; Monnet et al., 2015). However, whether The survivors were mainly smooth and weakly ornamented forms, while the late Permian selectivity occurred on other morphological species were dominated by coarsely ornamented forms. Contrary to previously recognized characters, e.g., shell ornamentation and aper- nonselective patterns, these results suggest a morphological selectivity of the Permian-Triassic ture shape, was not clear. Shell ornamentation crisis. Newcomers in the Griesbachian were mainly compressed and smooth forms. This mor- and aperture shape are important morphologi- phological shift from the coarsely ornamented ammonoids dominating the Changhsingian to cal parameters because they may significantly the smooth ammonoids dominating the Griesbachian possibly suggests an ecological turnover affect hydrodynamic properties (Chamberlain of ammonoids during the PTME. and Westermann, 1976; Hebdon et al., 2020). In our study, we performed morphometric analy- INTRODUCTION The PTME was the most severe crisis in the ses based on a comprehensive morphological Can we predict which kinds of organisms are Phanerozoic; it killed more than 80% of marine data set encompassing 127 ammonoid species to more likely to survive extinctions? The answer species (Stanley, 2016; Fan et al., 2020). It coin- quantify the morphological evolution of ammo- would be quite different with regard to back- cided with large environmental and climatic noids across the Permian-Triassic boundary and ground and mass extinctions. For example, taxa upheavals; e.g., global warming and oceanic test the morphological selectivity of the PTME. with wide geographic ranges can buffer against anoxia (e.g., Song et al., 2012; Sun et al., 2012). background extinction, but not for mass extinc- Therefore, the PTME can provide an excel- DATA AND METHODS tions (Dunhill and Wills, 2015). Mass extinc- lent deep-time experiment for testing selective We compiled a discrete morphological data tions in geological history usually act as a ran- extinction patterns. The PTME affected both taxa set from published literature that contained 87 dom nonselective pattern, affecting different with wide and narrow geographic ranges without Changhsingian and 40 Griesbachian ammonoid clades simultaneously and globally (Payne and selectivity (Payne and Finnegan, 2007; Dai and species (Table S1 in the Supplemental Material 1), Finnegan, 2007). However, some clades with Song, 2020); it did not show obvious selectiv- covering all valid genera known in this interval. specific ecological traits show higher resilience ity on bivalves with different lifestyles, feeding Taxa in open nomenclature or with problematic to mass extinctions than others; for example, types, or habitats (Huang et al., 2014). How- classification were also included when they had physiologically buffered groups were less ever, the PTME exhibited strong selectivity on a distinct morphology. We portioned the Gries- affected by the Permian-Triassic mass extinc- other specific groups and ecological traits; e.g., bachian ammonoids into two groups: survivors tion (PTME) than unbuffered groups (Bam- marine invertebrates had much higher extinc- and newcomers. Survivors were defined as initial bach et al., 2002). Greater understanding of the tion rates than chondrichthyan fishes (Vázquez postextinction species belonging to the surviving selectivity of mass extinctions can shed light on and Clapham, 2017). The degree of selectivity families and superfamilies; i.e., Otocerataceae, extinction mechanisms and predict the extinc- was thus highly variable among different clades, Episageceratidae, and Xenodiscidae (Wiedmann, tion risk of living species. ecological traits, and geographic ranges. 1973; Teichert and Rochester, 1986). Newcom- Ammonoids suffered a diversity bottleneck ers were all derived species and representatives *E-mail: [email protected] during the PTME, with the survival of only three of the newly originated families after the PTME; 1Supplemental Material. Figures S1 and S2, and Tables S1 and S2. Please visit https://doi .org/10.1130/GEOL.S.14582730 to access the supplemental material, and contact [email protected] with any questions. CITATION: Dai, X., Korn, D., and Song, H., 2021, Morphological selectivity of the Permian-Triassic ammonoid mass extinction: Geology, v. 49, p. 1112–1116, https:// doi.org/10.1130/G48788.1 1112 www.gsapubs.org | Volume 49 | Number 9 | GEOLOGY | Geological Society of America Downloaded from http://pubs.geoscienceworld.org/gsa/geology/article-pdf/49/9/1112/5387032/g48788.1.pdf by guest on 25 September 2021 tabulate venter rounded venter Figure 1. Representa- tives of Changhsingian and Griesbachian ammo- noids and their typical shell ornamentations. (A,B) Pseudotirolites acu- ticostatus from the Dalong Formation (Changhsin- gian), Guizhou, China. (C,D) Pseudogastrio- ceras szechuanense ventral keel striation from the Dalong Forma- C D tion (Changhsingian), Sichuan, China. (E) A B Tapashanites floriformis from the Dalong Forma- nodes width (W) tion (Changhsingian), Sichuan, China. (F,G) Vish- nuites pralambha from the lower Daye Formation (H) (Griesbachian), Guizhou, ) H I China. (H,I) Anotoceras (D nala from the lower Daye height Formation (Griesbachian), ribs Guizhou, China. (J,K) Ophiceras tibeticum from the lower Kangshare For- mation (Griesbachian), diameter South Tibet, China. umbilical E diameter (U) 5 cm F G J K i.e., Ophiceratidae, Proptychidae, Mullericerati- method is based on a two-dimensional morpho- sampling biases for SOV and SOR. We set a null dae, and a family incertae sedis species Anoto- space. It can be quantified by three parameters: hypothesis simulation wherein, given a random ceras nala. sum of range (SOR), sum of variance (SOV), extinction of species with 10,000 replicates, the Morphological characteristics employed and position of centroid (POC). Three theoreti- number of survivors is the same as the number in our study were based on the analysis by cal modes of extinction can lead to reductions in of empirical survivors. Then, we compared the McGowan and Smith (2007) with some modi- morphological disparity: random, marginal, and change of the centroid positions between the fications (see Table S2). These characteristics lateral extinctions. At the same extinction mag- null hypothesis and empirical survivors. The encompass conch geometry, ornamentation, nitude, SOR and SOV will show the smallest distance between the centroids was calculated shape of the aperture and ontogeny (Fig. 1). decrease in random extinction mode, an inter- by Euclidean distance using their two NMDS Size was not included in this analysis because mediate decrease in lateral extinction mode, coordinates. The simulations were performed ammonoid shells were usually damaged dur- and the largest reduction in marginal extinction using R version 3.5.3 (https://cran.r-project.org/ ing postmortem transportation and taphonomic mode; POC will not show prominent changes in bin/windows/base/old/3.5.3/). processes. We usually coded the studied spe- random and marginal modes, but it will exhibit cies based on its holotype, when it was well remarkable change in lateral mode. RESULTS preserved. Non-holotype specimens were used We used the nonmetric multidimensional The morphospace of the Changhsingian in case of incomplete preservation of the holo- scaling (NMDS) method to construct an ammo- and Griesbachian ammonoids showed signifi- type. Intraspecific variation was not considered noid morphospace, because this is widely cant differences (Fig. 2A). The one-way per- here owing to three reasons: (1) most of the adopted for analyzing discrete morphological mutational multivariate analysis of variance studied species were described on the basis of data. Two distance metrics (i.e., Euclidean and (PERMANOVA) test of their morphological a few specimens; (2) adding more specimens of Gower) were used to calculate pairwise